Plastic and Reconstructive Surgery

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Plastic & Reconstructive Surgery:
doi: 10.1097/PRS.0000000000000020
Cosmetic: Original Articles

In Vitro and In Vivo Investigation of the Influence of Implant Surface on the Formation of Bacterial Biofilm in Mammary Implants

Jacombs, Anita B.Sc.(Hons.),M.B.B.S.; Tahir, Shamaila M.B.B.S.; Hu, Honghua Ph.D.; Deva, Anand K. F.R.A.C.S.; Almatroudi, Ahmad B.Sc., M.P.H.; Wessels, William Louis Fick M.B.B.S.; Bradshaw, David A. M.B.B.S.; Vickery, Karen B.V.Sc.(Hons.), Ph.D.

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Author Information

Sydney, New South Wales, Australia

From the Surgical Infection Research Group, Australian School of Advanced Medicine, Macquarie University.

Received for publication June 20, 2013; accepted September 11, 2013.

The first two authors should be considered co–first authors.

Presented in part at the Technology in Plastic Surgery Meeting, in San Francisco, California, May 31 through June 2, 2013 and selected for presentation at The Aesthetic Meeting 2014, in San Francisco, California, April 24 through 29, 2014.

Disclosure: Dr. Deva and Dr. Vickery are consultants to Allergan, Mentor (Johnson & Johnson), and Kinetic Concepts, Inc. They have previously coordinated industry-sponsored research for these companies relating to both biofilms and breast prostheses. The remaining authors have no financial interests to disclose.

Anand K. Deva, B.Sc.(Med.), M.B.B.S., M.S., Surgical Infection Research Group, Australian School of Advanced Medicine, Macquarie University, Suite 301, 2 Technology Place, Macquarie Park, New South Wales 2109, Australia,

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Background: Capsular contracture remains the most common complication following breast augmentation surgery, and evidence suggests that bacterial biofilm on the implant surface is responsible. The authors investigated whether the interaction of bacterial biofilm with implants independently determines progression to capsule formation. They also studied the rate of bacterial growth and adhesion to implants.

Methods: Sixteen adult female pigs had 121 breast implants inserted. Sixty-six implants—23 smooth and 43 textured—were inoculated with a human strain of Staphylococcus epidermidis and received no other treatment. After an average period of 19 weeks, Baker grading was performed and implants were retrieved. For the in vitro study, samples underwent both quantitative bacterial analysis and imaging using confocal laser scanning and scanning electron microscopy.

Results: At explantation, there was no significant difference (p = 1.0) in the presence of capsular contracture (Baker grade III and IV) between smooth (83 percent) and textured implants (84 percent). Biofilm was confirmed on 60 of the 66 capsules. Capsules from smooth and textured implants had the same number of infecting bacteria (textured: 3.01 × 108 bacteria/g; smooth: 3.00 × 108 bacteria/g). In vitro, the surface of textured implants showed 11-, 43-, and 72-fold more bacteria at 2, 6, and 24 hours, respectively, compared with smooth implants (p < 0.001). These findings were confirmed by imaging analysis.

Conclusions: These results show that textured implants develop a significantly higher load of bacterial biofilm in comparison with smooth implants. Furthermore, in vivo, once a threshold of biofilm forms on either smooth or textured implant surfaces, there seems to be an equal propensity to progress to capsular contracture.

Breast augmentation and reconstruction using breast implants are among the most common procedures performed in plastic surgery.1 In 2011, over 310,000 breast augmentation procedures were performed in the United States alone.2

Contracture of the periprosthetic capsule with associated implant distortion, abnormal firmness, and pain remains the most common complication following breast augmentation.1,3 A number of theories have been put forward for the genesis of capsular contracture. The role of subclinical infection, however, has gained support from both clinical and preclinical studies, and there is now wide acceptance that bacterial biofilm on the surface of implants is the principal pathogenic pathway to development of capsular contracture.3–8

Texturization of the implant surface and its role in preventing contracture were first proposed following the introduction of polyurethane foam–covered implants. The next generation of texturization was introduced in the late 1980s, using a number of techniques to modify the external silicone shell.3,9 Several initial studies inserting one smooth and one textured implant per patient yielded differing outcomes, with some reporting reduced contracture rates with textured implants10 and others reporting no difference.9,11 Subsequently, several randomized controlled trials have shown more consistent results, with textured implants showing lesser rates of capsular contracture.12,13 There are now 10 published randomized controlled or split breast studies that are evenly divided as to whether texturization shows benefit1,10,13–15 or confers no difference.6,9,11,12,16 Texturization of the surface of implants has been shown to have biological benefits in enhancing biocompatibility and achieving optimal integration of living host and the alloplast.17 These effects include enhancing tissue adhesion, growth and proliferation of host blood supply, enhancement of cellular migration, and fibroblast adhesion.18,19

With this background in mind, we sought to use our well-established porcine model of capsular contracture to investigate whether the presence of a smooth or textured outer surface offers any advantages in preventing both biofilm formation and capsular contracture following deliberate bacterial inoculation. We also designed an in vitro attachment assay to determine the influence of implant surface on the growth and attachment of bacterial biofilm.

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Approval for the all study protocols was obtained from the University of Sydney Animal Ethics Committee.

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Surgical Procedure

A total of 16 adult, female, nonlactating, domestic Large White pigs (Sus domesticus) weighing approximately 350 kg each were used. One hundred twenty-one implants (average diameter, 3 cm) were inserted, with each pig receiving between six and eight implants. Of these, 66 implants (23 smooth and 43 textured) were all inoculated with an average of 105 colony-forming units of a human strain of Staphylococcus epidermidis and received no other treatment. These 66 implants were used in this study.

Implants were inserted into submammary pockets as described by Tamboto et al.4 The implants were left in situ for an average of 19 weeks, after which clinical assessment by Baker grading was performed.

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Baker Grade

Contracture of the 66 implants was assessed blinded using the four-grade Baker scale20 while the implants were in situ.

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Total Number of Bacteria in Capsules and Attached to Implants

The total numbers of bacteria in capsular tissue surrounding 14 smooth and nine textured implants and the numbers of bacteria attached to 11 smooth and nine textured implants were determined by real-time quantitative polymerase chain reaction using universal eubacterial primer 16S rRNA_341F 5′-CCTACGGGAGGCAGCAG-3′ and 16S rRNA_534R 5′-ATTACCGCGGCTGCTGG-3′ to amplify a 194–base pair amplicon of 16S rRNA gene of all bacteria as described previously.21

Between 50 and 100 mg of capsular tissue and between 40 and 100 mg of implants were digested using a combination of proteinase K and lysozyme digestion, and the genomic DNA was extracted using phenol/chloroform extraction followed by ethanol precipitation as described previously.21 The number of bacteria in each tissue sample was normalized to the amount of tissue digested by real-time quantitative polymerase chain reaction of the 18S ribosomal RNA reference gene (GenBank accession no. AY265350.1) using the primer pair 18S rRNA_756F 5′-GGTGGTGCCCTTCCGTCA-3′ and 18S rRNA_877R 5′-CGATGCGGCGGCGTTATT-3′ as described previously.21

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Scanning Electron Microscopy

The presence of biofilm was confirmed visually on all implants and capsules using scanning electron microscopy. Samples were fixed in 3% glutaraldehyde, dehydrated through alcohol, and then immersed in hexamethyldisilazane (Sigma-Aldrich, St. Louis, Mo.) 50% for 10 minutes and 100% for 10 minutes, three times, before being aspirated dry and evaporated dry overnight. They were mounted on metal stubs with carbon tabs and coated with 20-nm gold film in a sputter coater. The samples were imaged using a JEOL 6480LV scanning electron microscope (JEOL Ltd., Tokyo, Japan) with a voltage of 10 kV and a viewing distance of 20 mm.21

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In Vitro Assay

Fourteen miniature, textured, 2-cm-diameter and 14 miniature, smooth, 2-cm breast implants were incubated in 20 ml of 10% tryptone soya broth (Oxoid, Cambridge, United Kingdom) containing 5.8 × 106 colony forming units/ml of S. epidermidis, originally obtained from a contracted human breast4 at 37°C. In addition, eight separate pieces of implant shell (four textured and four smooth) were included in the incubation chamber for the purposes of imaging.

Four implants of each type were removed for quantitative bacterial analysis from the chamber at 2, 6, and 24 hours for colony-forming unit determination. They were washed twice in phosphate-buffered saline and then placed in 20 ml of phosphate-buffered saline to be subjected to sonication for 20 minutes followed by 1 minute of vigorous shaking as described previously.5

Quantitative numbers of bacteria attached to whole implants were determined by 10-fold serial dilution and subsequent plate culture. Bacteria attached to the implant sections were visualized by using confocal microscopy and scanning electron microscopy.

For confocal microscopy, one implant of each type was removed from the chamber at the three time points. Sections of the implant were stained with a DNA stain Live/Dead BacLight Bacterial Viability Kit 7012 (Molecular Probes, Life Technologies, Grand Island, N.Y.) according to the manufacturer’s instructions. Live cells appeared green and dead cells appeared red because of preferential binding of propidium iodide. Stained samples were examined using an Olympus FluoView 300 inverted confocal laser scanning microscopy system (Olympus Corp., Tokyo, Japan). Implants for scanning electron microscopy were prepared and imaged as described above.

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Statistical Analysis

The Fisher’s exact test was used to examine differences in contraction rate between smooth and textured implants using the statistical package Sigma Plot 13 (Systat Software, Inc., San Jose, Calif.). The t test was used to examine for differences in the number of bacteria associated with contracted implants compared with noncontracted implants and for comparing the number of bacteria associated with textured and smooth implants. The data for the in vivo study were distributed normally and had equal variance. The data for the 6- and 24-hour time point analysis in vitro had to be transformed to ensure normality and equal variance. The Mann-Whitney rank sum test was used to examine for differences in the number of bacteria attached to different implants and in capsular tissue surrounding those implants.

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In Vivo Study

No pig exhibited systemic signs of infection relating to either bacterial inoculation and/or the presence of a surgical implant.

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Baker Grade

There were no significant differences between smooth and textured implants regarding the proportion of breasts that developed contracture (Baker grade III and IV) following artificial inoculation of S. epidermidis (p = 1.0). At explantation, 83.7 percent of the capsules around the textured implants and 82.6 percent of the capsules around the smooth implants had capsular contracture (Baker grade III and IV). Seven (16.3 percent) of the 43 textured and four (17.4 percent) of the smooth implants had no clinical capsular contracture (Baker grade I and II) (Table 1).

Table 1
Table 1
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Total Number of Bacteria in Capsules and Attached to Implants

Although all implant pockets were inoculated with the same number of bacteria, those that went on to develop contracture had 250 percent more bacteria associated with them than those that failed to develop contracture. In artificially inoculated implant pockets, there was no significant difference in total bacterial numbers in capsular tissue surrounding smooth (n = 14) and textured implants (n = 9). Capsular tissue surrounding textured implants contained an average of 3.00 × 108 bacteria/g of tissue and tissue surrounding smooth implants contained an average of 3.01 × 108 bacteria/g of tissue.

Interestingly, there were 20-fold more bacteria attached to the textured implants (1.18 × 108 bacteria/g of implant) than smooth implants (5.75 × 106 bacteria/g of implant). This difference was significant (p = 0.006).

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Scanning Electron Microscopy

Bacterial biofilm was confirmed by scanning electron microscopy on all of the Baker grade III/IV implant capsules. We were unable to confirm biofilm on four capsules from Baker grade I and II implants. Most of the capsules displayed thick biofilm, with loss of the normal capsule fibrous architecture, over a large area of the imaged specimen (Fig. 1, above). Coccoid bacteria embedded in biofilm exopolymeric substances were frequently identified. The remaining capsules showed occasional or patchy biofilm, and normal fibrous capsule architecture was maintained (Fig. 1, below). More bacteria were attached to the surface of textured implants compared with smooth implants (Fig. 2).

Fig. 1
Fig. 1
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Fig. 2
Fig. 2
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In Vitro Study


Our analysis showed that at 2 hours, the mean number of bacteria attached to the textured implants was 3.8 × 106 (range, 1.6 to 6.6 × 106) as compared with 3.4 × 105 (range, 1.6 to 6.3 × 105) on smooth implants. This difference was significant (p = 0.015). At the 6-hour time point, the number of bacteria attached to the textured implant had increased by a factor of 43-fold on the textured implants compared with the smooth implants [6.8 × 107 (range, 6.0 to 7.5 × 107) for textured versus 1.6 × 106 (range, 0.8 to 2.4 × 106) for smooth]. At the 24-hour time point, the textured implants had 72 times the number of bacteria attached to their surface compared with the smooth implants [6.0 × 109 (range, 2.8 to 6.4 × 109) for textured versus 8.2 × 107 (range, 6 to 12.8 × 107) for smooth]. The differences at the 6- and 24-hour time points were highly significant (p < 0.001). These data are summarized in Figure 3.

Fig. 3
Fig. 3
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Confocal microscopy confirmed that the number of bacteria attached to textured implants was far greater than the number attached to smooth implants at each time point (Fig. 4). Scanning electron microscopy of the smooth and textured outer shells at 24 hours also confirmed our findings on microbiology, showing dense and mature biofilm on the surface of textured implants and patchy biofilm on the surface of smooth implants (Fig. 5).

Fig. 4
Fig. 4
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Fig. 5
Fig. 5
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In the 50 years since the initial silicone breast implant was used surgically for breast augmentation, capsular contracture has remained the most common complication, often requiring further surgical intervention.3,22,23 The cause of capsular contracture remains poorly understood but is likely to be multifactorial in origin.3,23 However, a recent large clinical study by Rieger et al.24 has confirmed that Baker grade of contracture directly correlates with the number of bacteria identified by sonication and culture. These findings further support the subclinical infection theory. In this study, we investigated whether a smooth or textured implant surface offered any advantage in preventing the development of capsular contracture in artificially inoculated pockets of an in vivo pig model.

There was no significant difference in the rate of capsular contracture between smooth surface implants and textured surface implants following deliberate inoculation with human S. epidermidis. Following inoculation, 82 percent of breasts implanted with textured prostheses and 83.4 percent of breasts implanted with smooth prostheses developed contracture. These rates are consistent with our previous findings.4 Contracted breast capsules had 250 percent more bacteria compared with noncontracted capsules. These data once again reinforce the pathway from initial contamination of breast implants with bacteria progressing to established biofilm and subsequent contracture.

The subclinical infection theory has been further validated by these data. We have shown once again that deliberate inoculation with S. epidermidis results in progression to biofilm and contracture in approximately 80 percent of implants. It is likely that there is a threshold of biofilm load, which, once crossed, leads to significant potentiation of capsule formation. This threshold seems to be independent of whether the implant is smooth or textured. The finding of higher numbers of bacteria on textured implants (up to 20-fold more in vivo and 72-fold in vitro) is consistent with the subclinical infection hypothesis, as additional bacteria above this threshold results in the same outcome (i.e., development of contracture) (Fig. 6).

Fig. 6
Fig. 6
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The Baker grading was consistent with our scanning electron microscopic findings, which demonstrated either obvious thick biofilm or patchy biofilm in all but six textured implants. Four of the six implants in which we failed to visually confirm biofilm were culture-positive, demonstrating the patchy nature of biofilm infection and likely sampling error when using scanning electron microscopy as a sole diagnostic test for the presence of biofilm.

These results show that both implant surface types will readily form biofilm under experimental conditions using deliberate inoculation of S. epidermidis. A constant finding was that, as the degree of contracture increased, as measured by Baker grading and tonometry, capsular architecture became less organized and the collagen fibers were covered in biofilm exopolysaccharide (Fig. 1). This effect was seen in capsules from around both smooth and textured implants. A further long-term study to investigate the correlation between the amount of biofilm load and degree of capsular contracture using the porcine model is currently underway.

The in vitro analysis has demonstrated clearly that the presence of a textured outer shell on breast implants encourages a higher rate of biofilm growth. This finding is consistent with a growing body of research from industry and more specifically from investigations on biofouling of metal and plastic surfaces. Biofouling refers to an undesirable development of biofilm on a membrane surface, involving accumulation of deposited microbial cells embedded within a matrix of extracellular polymeric substances.25 Biofouling has become increasingly recognized as a leading cause of failure in a range of industrial and domestic areas, including water purification systems, hydraulics, home appliances, and food processing.26–28

Wenzel29 was the first to note that rough surfaces were more susceptible to wetting because of an increase in both contact angle and surface area. As predicted by Wenzel, as the surface complexity or roughness increases, so too does the propensity for biofilm growth.30

Substrates with varying roughness have now been subjected to biofilms in vitro. Arnold and Bailey31 have demonstrated that electropolished steel has less propensity for early biofilm attachment and formation compared with rough steel substrates. Myint et al.32 have similarly shown that for polyamide nanofiltration membranes, increased surface roughness potentiates initial biofilm cell attachment, aggregation, and colony formation.

The finding that textured breast implants significantly potentiate biofilm formation compared with smooth implant surfaces has implications for both clinicians and scientists. As the evidence for subclinical infection as a potentiator for contracture increases, surgeons using textured implants need to be especially aware of strategies to prevent the access of bacteria to the implant at the time of surgical implantation. Nipple shields,33 pocket irrigation,3,34 no-touch insertion,35 perioperative antibiotic prophylaxis,36 and avoiding the trans areolar incision37 have all been recommended as strategies for reducing the risk of bacterial contamination at the time of breast implant insertion. It would be prudent, especially when using textured implants, to recommend mandatory use of these strategies to prevent the initial attachment and subsequent formation of bacterial biofilm on breast implants. The biological advantages of texture, including better tissue ingrowth and potentially less contracture, need to be balanced by the higher risk of bacterial contamination. Surgeons should be aware of this risk and modify their intraoperative strategy to reduce the likelihood of bacterial contamination of breast implants.

For industry and researchers alike, the search for the ideal combination of surface morphology and intrinsic bacterial resistance should be made a priority. The development of this technology would have implications not only for breast prostheses but also for all other implantable medical devices. In orthopedic surgery, for example, failure of hip and knee arthroplasties has been shown to be attributable to biofilm infection, and strategies for intraoperative prevention have shown early promise in reducing the risk of device-associated infection.38

The goal to develop an alloplastic surface that resists or limits bacterial adhesion and biofilm formation continues. A number of surface modification techniques have been applied to biomaterials, including antiadhesive, antiseptic, and antibiotic coatings; surface grafting; chemical modification; and biological membranes.39–41 The techniques aim to create a new interface between the host and the alloplast by modifying topography, surface functional groups, hydrophobicity, and surface charge, and improving the ability of the surface to kill bacteria. The successful design of a truly biofilm-resistant surface, however, remains a significant challenge because of the variation in required physical properties of the biomaterials, the variety of design and regulatory demands for medical devices, and the changing patterns of resistance of the microbial population.

The finding of an increased number of bacteria attached to the surface of the textured implant is novel. It will be interesting to see whether this higher bacterial load is responsible for chronic immune activation, which in turn may predispose to potential lymphocytic hyperplasia.

The complex interactions between the potentiators and suppressors at play in this hypothesis are not yet fully understood. In this study, we have investigated the interactions between subclinical infections and surface texture. Almost all capsules demonstrated positive findings of bacterial biofilm at the time of removal, with neither surface type demonstrating any reduction in capsular contracture rates. These results suggest that the potentiating stimulus of subclinical infection far exceeds any potential advantage that may be conferred by implant surface type.

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In breast implants, although textured implants may confer better tissue ingrowth, they also have been shown to potentiate the early and rapid formation of S. epidermidis biofilm in vivo and in vitro compared with smooth implants. The use of textured implants should especially be combined with stringent intraoperative attention to the prevention of bacterial contamination to reduce the risk of biofilm formation and subsequent capsular contracture.

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This study was funded in part by Mentor Texas LP and Allergan Sales, LLC. The authors thank Debra Birch, Microscopy Department, School of Biological Sciences, Macquarie University, for providing expertise in electron microscopy. Karen Vickery, B.V.Sc.(Hons.), Ph.D., was in receipt of a Macquarie University Vice Chancellor Innovation Fellowship; Anita Jacombs, B.Sc.(Hons.), Grad.Dip., M.B.B.S., was in receipt of a National Health and Medical Research Council Postgraduate Scholarship; and David A. Bradshaw, M.B.B.S., was in receipt of an Australian Postgraduate Scholarship from the Australian Government.

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